Sleep and Daytime Function in People with Spinal Cord Injury

Study Design: Cross-sectional cohort study. Objectives: To determine the role of sleep-disordered breathing (SDB), insomnia symptoms and sleep quality in the daytime function and quality of life of veterans with spinal cord injury (SCI). Setting: A Veterans Administration (VA) medical center in the Midwestern US. Methods: Thirty-eight male veterans with SCI (22 cervical, 16 thoracic; mean [SD] age = 62.9[9.5] years) completed baseline assessments within a larger clinical trial. Measures assessed sleep apnea severity (apnea-hypopnea index, AHI), insomnia symptoms (Insomnia Severity Index, ISI), self-reported sleep quality (Pittsburg Sleep Quality Index, PSQI), daytime sleepiness (Epworth Sleepiness Scale, ESS), fatigue (Flinders Fatigue Scale, FFS), depression (Patient Health Questionnaire-9 item, PHQ-9 excluding sleep item), functioning (Spinal Cord Independence Measure, SCIM), and quality of life (World Health Organization Quality of Life, WHOQOL-BREF). Bivariate correlations (alpha p<.05) were used to assess relationships between sleep (AHI, ISI, PSQI, ESS) and function (FFS, PHQ-9, SCIM, WHOQOL-BREF). Results: Mean AHI was 29.9(26.6), mean ISI was 9.38(6.2), mean PSQI was 9.0(4.6), and mean ESS was 7.0(5.2). There were no significant relationships between AHI and function measures. Significant relationships emerged between ISI and PHQ-9, some WHOQOL-BREF subscales, and SCIM as well as between PSQI and FFS, PHQ-9, and some WHOQOL-BREF subscales. Conclusions: Among Veterans with SCI, insomnia symptom severity and poor sleep quality were associated with worse functioning, whereas SDB severity was not. Insomnia and poor sleep quality represent modifiable contributors to poor daytime function. Research evaluating the impact of evidence-based insomnia treatments among individuals living with SCI is warranted.


Introduction
Sleep disorders, such as sleep-disordered breathing (SDB) and insomnia disorder, are experienced by individuals living with spinal cord injury (SCI) at elevated rates as compared to the general population.(1)An estimated three-quarters of individuals with SCI meet the criteria for SDB, (2)(3)(4) and symptoms of insomnia are reported by the majority of individuals with spinal cord injuries.(5) Sleep problems may contribute to daytime symptoms such as fatigue, worse mental health symptoms, poor cognitive function, and impaired quality of life (6)(7)(8) in individuals with SCI who are already facing numerous challenges in their daily functioning.SDB, the term for sleep disorders such as obstructive sleep apnea (OSA) that involve reduced or cessation of breathing during sleep, is often associated with myriad comorbidities and risk for significant health events (e.g., cardiovascular disease, stroke).However, insomnia may also be a cause for concern in the SCI population.Insomnia disorder, defined as chronic, habitual difficulty falling and/or staying asleep combined with daytime functional impairment, (9) can result in difficulty managing symptoms of other health conditions such as SCI and poor quality of life.
Our previous work demonstrated that the severity of insomnia symptoms is associated with elevated mental health symptoms of depression, anxiety, and posttraumatic stress disorder (PTSD) in individuals with spinal cord injuries and diseases (SCI/D).(10) Additionally, we found that both worse insomnia and worse sleep quality were linked to elevated daytime fatigue and reduced quality of life in individuals with multiple sclerosis (MS), (11) a spinal cord disease with functional challenges that may parallel those experienced by individuals with SCI.
While it is known that individuals with SCI have elevated rates of disturbed sleep, few studies have examined the relationships between sleep and functioning in individuals with SCI.Therefore, this investigation aimed to determine the relative contribution of SDB, insomnia symptoms, and self-reported sleep quality to daytime function and quality of life in veterans with SCI.We hypothesized that more severe SDB, worse insomnia symptoms, and worse sleep quality would be associated with worse daytime functioning.

Methods
We analyzed data collected from a subset of participants enrolled in a larger clinical trial (NCT02830074) related to the treatment of SDB for individuals with either SCI or spinal cord disease (SCD).(12) Baseline assessments consisted of in-laboratory polysomnography (PSG) and questionnaires that assessed both daytime and nighttime functioning.Questionnaires were presented verbally via standardized scripts and visual response prompts to mitigate the impact of physical limitations experienced by many participants that could increase the burden of written or computer-based questionnaires.
For the current analyses, we utilized data from the 38 veterans with SCI enrolled in the trial.The Institutional Review Board at Wayne State University in Detroit, MI, reviewed and approved the study.The VA Northeast Ohio Healthcare System also approved the study.A waiver of documentation of consent was obtained for screening.All participants gave written or witnessed verbal consent for those with limited upper extremity mobility.
Study procedures took place at the John D. Dingell Veterans Administration Medical Center (JDDVAMC).
Inclusion criteria for the parent study were veterans with a spinal cord injury who were at least 3 months post-injury and were receiving care at one of the participating medical centers.Exclusion criteria were: mechanical ventilation, current use of positive airway pressure therapy (PAP) for SDB, clinical contraindication preventing PAP use, recent health event (e.g., recent stroke, recent surgery or hospitalization) that would likely impair sleep, less than 90 days sobriety from alcohol or substance abuse, selfreported inability to fully participate in study procedures (e.g., due to significant illness), or lack of capacity to self-consent (e.g., dementia).

Demographics:
Demographic data such as age, gender, race/ethnicity, marital status, employment status, living situation, and income were collected to describe the study sample.

Sleep Measures:
A single night of in-laboratory polysomnography (PSG) was performed to determine SDB diagnosis, severity via apnea hypopnea index (AHI: number of apneas and hypopneas per hour of sleep), and sleep efficiency (PSG-SE: percentage of time in bed spent asleep).(13) PSGs were scored according to AASM scoring criteria by trained technologists meeting AASM Interscorer reliability standards (13) and scoring was confirmed by a board-certified sleep medicine physician.PSG data were unavailable for 3 participants (n=35 for AHI and PSG-SE variables).
The Insomnia Severity Index (ISI) (14) was used to assess insomnia severity.
The ISI is a subjective 7-item questionnaire that evaluates the quality of sleep, satisfaction with sleep, insomnia interference in daily functioning, severity of insomnia symptoms, distress caused by sleep problems, and if the insomnia is noticeable to others.The tool uses a Likert scale of 5 points.A score below 7 indicates no clinically significant insomnia, 8-14 as subthreshold insomnia, 15-21 as clinical insomnia (moderate severity), and 22-28 as clinical insomnia (severe).
The Pittsburgh Sleep Quality Index (PSQI) is a self-report questionnaire comprising 18 items assessing sleep habits and symptoms (i.e., sleep quality, latency, duration, efficiency, disturbances, daytime function, and medication use) over the past week.It is scored using both a 4-item Likert scale and open-ended questions converted to subscale scores.Higher scores are indicative of acute sleep disturbances.The PSQI has been shown to be a valid and reliable measure of good vs. poor sleepers (15).The three-subscale scoring system was used due to more favorable psychometric properties.(16)

Measures of Daytime Symptoms:
The Epworth Sleepiness Scale (ESS) ( 17) is a questionnaire that assesses the subjective likelihood of dozing off during 8 different daily activities such as reading, watching TV, or sitting as a passenger in a car on a scale from 0 (no chance of dozing) to 3 (high chance of dozing).The questionnaire is scored from 0-24 with a score over 10 indicating clinically significant sleepiness.The Spinal Cord Independence Measure (SCIM) ( 20) is a 19-item questionnaire that assesses 3 domains of function for individuals with spinal cord injuries to determine their level of independence and measure functional progress.The first domain is selfcare, which assesses feeding, bathing, dressing, and grooming (scored 0-20).The second domain is respiration and sphincter management, which consists of respiration and bladder and bowel management, and use of the toilet (scored 0-40).The third domain is mobility, which assesses tasks such as transfers from bed to wheelchair or wheelchair to toilet and mobility indoors and outdoors (scored 0-40).The total SCIM score ranges from 0-100, with higher scores indicating greater independence in functioning and assisting clinicians in developing a treatment plan, setting functional goals, and monitoring progress.

Quality of Life Measure:
The World Health Organization Quality of Life: Brief Version (WHOQOL-BREF)

Results
Table 1 shows the characteristics of study participants.The mean age was 63 years, and 100% of the 38 participants were male.Table 3 summarizes the correlations between sleep, daytime symptoms, functioning, and quality of life measures.There were no significant relationships between AHI and any daytime symptoms, SCI-related functioning, or quality of life outcomes.Worse objective sleep quality (PSG-SE) only correlated with poorer SCIrelated functioning (SCIM).Significant relationships were observed between greater insomnia symptoms (ISI) and worse depression symptoms (PHQ-9), quality of life (both the Physical Health and Environment subscales of the WHOQOL-BREF), and functioning (SCIM).Lower self-reported sleep quality (PSQI) was associated with worse fatigue (FFS), depression symptoms (PHQ-9), and quality of life (three subscales of the WHOQOL-BREF: Physical Health, Psychological Health, and Environment subscales).

Summary of Findings
These analyses aimed to expand the existing literature on the interplay between sleep (specifically, SDB, insomnia symptoms, and perceived sleep quality), functioning, and quality of life in Veterans with SCI.Our study demonstrated that veterans living with SCI have high rates of sleep disturbance (insomnia symptoms and self-reported sleep quality), which was significantly associated with worse daytime function and quality of life.However, our hypothesis that sleep apnea severity (AHI) would also be associated with daytime symptoms, quality of life, and functioning outcomes was not confirmed.
Our data suggest poor sleep and insomnia symptoms, regardless of SDB status, are critical determinants of daytime impairments.

Determinants of Sleep Quality in Veterans Living with SCI
We found that self-reported measures of sleep quality, specifically PSQI and ISI, were related to depression, quality of life, and SCIM.Depression is common in individuals living with SCI, (24) and they often experience lower life satisfaction.(25) The determinants of depression in this population are not clear; however, poor sleep quality can result in less engagement in daily activities and rehabilitation, decreasing quality of life and overall independence, (26) 29) Therefore, poor sleep may be a modifiable risk factor to improve not only general function but also mood and mental health conditions such as depression in veterans with SCI.

Limitations
Several methodological considerations may affect the interpretation of our findings.First, the study sample size was small, which precluded multivariable modeling and increased the risk of type 2 errors.As such, we avoided interpreting any one statistical test but focused on the pattern of results (i.e., that insomnia but not SDB severity was associated with functional impairments).Second, the diagnostic sleep studies were conducted in a sleep laboratory and do not represent typical sleep in the home environment.However, in-laboratory polysomnography remains the gold standard for assessing sleep architecture and diagnosing SDB among individuals with musculoskeletal abnormalities, such as those with SCI.Third, the generalizability of the study is limited to male veterans with SCI, which may not be representative of women or non-veterans with SCI.Finally, circadian rhythm disorder is common in those with cervical spinal cord injury owing to a lack of melatonin secretion in this population, and our study did not include a formal assessment of circadian tendencies or disorders.(30)

Implications of Findings
Sleep quality and disorders should be prioritized in the overall comprehensive care of individuals living with SCI.Investigating causes of poor sleep quality in individuals living with SCI will include causes of sleep fragmentation (including SDB), poor sleep quality, and insomnia disorder, with the aim of identifying modifiable risk factors.Cognitive behavioral therapy for insomnia (CBT-I) is the first-line treatment for chronic insomnia disorder; however, CBT-I has not been systematically evaluated among patients with SCI, and adaptations to standard treatment components may be necessary.For example, stimulus control instructs a patient to move out of the bedroom if unable to fall asleep; however, this can be a significant challenge for those living with SCI, and adaptations that do not increase the burden on family care providers are needed.

Conclusion
Sleep disturbance, specifically insomnia symptom severity and poor sleep quality, were associated with worse daytime functioning in Veterans with SCI.However, SDB was not linked to any functioning measures.Improvement of insomnia and sleep quality may benefit daytime function; therefore, assessing evidence-based treatments for insomnia, such as cognitive-behavioral therapy, is necessary in individuals with SCI.

Flinder' s
Fatigue Scale (FFS) (18) is a 7-item questionnaire that assesses the extent of daily fatigue in individuals with insomnia in frequency, severity, and impairment to daytime functioning.FFS scores range from 0 to 31.A score of 13-15 is borderline, 16-20 is moderate, and greater than 21 is severe fatigue.The Patient Health Questionnaire-9 (PHQ-9) (19) is a commonly used questionnaire that assesses clinical depression symptoms in outpatient settings.It is scored from 0 to 27, and a score above 20 indicates clinically significant depression.

( 21 )
is a self-report questionnaire assessing quality of life (QOL).The measure is an adapted, shorter version of the WHOQOL-100 questionnaire.It consists of 26 items that assess QOL in domains of physical health, psychological health, social relationships, and environment.Each question is scored on a 5-point Likert scale, with the mean score of each question determining the domain score and with higher scores indicative of higher QOL.Data Analysis: Data were entered into REDCap (Research Electronic Data Capture) (22) and exported to Stata 17.0 (23) for analysis.Descriptive statistics were calculated for all study variables to contextualize the study sample.Relationships between sleep measures (AHI and SE from PSG, ISI, and PSQI) and daytime function (ESS, FFS, PHQ-9, WHOQOL, and SCIM) were assessed using bivariate correlations.An alpha level of ≤ .05constituted statistical significance.
measures.Of the 38 participants, sleep-disordered breathing (AHI ≥ 15 events/hour) was present in n=22 participants, and the sample mean AHI score was 30 events/hour.Insomnia, defined as ISI score ≥ 15, was present in n=8 (21.05%) participants.The sample mean ISI score was 9. Poor sleep quality, defined as PSQI score ≥ 5, was endorsed by n=28 (73.68%) participants.The sample mean PSQI score was 9.
which may contribute to depression symptoms.Rehabilitation literature corroborates our findings that poor sleep can lead to high levels of fatigue that diminishes engagement in daily meaningful activities for individuals with SCI.(27) Continued poor sleep can result in limited engagement in rehabilitation activities, resulting in decreased daily functioning of those with SCI.(28) Sleep disturbance and poor sleep patterns can increase the energy and time required for daily SCI care and participation in functional tasks, thereby limiting energy for engagement in other meaningful activities.Rehabilitation clinicians may focus on other risk factors for poor outcomes in those with SCI, such as bowel/bladder, pressure sores, and decreased function.Unfortunately, sleep may be overlooked in the rehabilitation setting despite the knowledge that poor sleep is linked to negative outcomes in individuals with SCI.(

Table 2
summarizes the sleep, daytime symptoms, functioning, and quality of life